Sex-specific innate immunity and ageing in long-lived fresh water turtles (Kinosternon flavescens: Kinosternidae)

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2023-03-09
Authors
Kutz, Greta A.
Holden, Kaitlyn G.
Reinke, Beth
Iverson, John B.
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© The Author(s) 2023
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Ecology, Evolution and Organismal Biology
Abstract
Background
The progressive deregulation of the immune system with age, termed immunosenescence, has been well studied in mammalian systems, but studies of immune function in long-lived, wild, non-mammalian populations are scarce. In this study we leverage a 38-year mark-recapture study to quantify the relationships among age, sex, survival, reproductive output and the innate immune system in a long-lived reptile, yellow mud turtles (Kinosternon flavescens; Testudines; Kinosternidae).
Methods
We estimated rates of survival and age-specific mortality by sex based on mark-recapture data for 1530 adult females and 860 adult males over 38 years of captures. We analyzed bactericidal competence (BC), and two immune responses to foreign red blood cells - natural antibody-mediated haemagglutination (NAbs), and complement-mediated haemolysis ability (Lys) - in 200 adults (102 females; 98 males) that ranged from 7 to 58 years of age captured in May 2018 during their emergence from brumation, and for which reproductive output and long-term mark-recapture data were available.
Results
We found that females are smaller and live longer than males in this population, but the rate of accelerating mortality across adulthood is the same for both sexes. In contrast, males exhibited higher innate immunity than females for all three immune variables we measured. All immune responses also varied inversely with age, indicating immunosenescence. For females that reproduced in the preceding reproductive season, egg mass (and therefore total clutch mass) increased with age,. In addition to immunosenescence of bactericidal competence, females that produced smaller clutches also had lower bactericidal competence.
Conclusions
Contrary to the general vertebrate pattern of lower immune responses in males than females (possibly reflecting the suppressive effects of androgens), we found higher levels of all three immune variables in males. In addition, contrary to previous work that found no evidence of immunosenescence in painted turtles or red-eared slider turtles, we found a decrease in bactericidal competence, lysis ability, and natural antibodies with age in yellow mud turtles.
Background
Ageing in many vertebrate systems is characterized by organismal senescence – declining efficiency and performance of physiological and cellular processes [1] leading to declining age-specific survival and fertility with advancing age [2]. Studies of ageing in wild populations of vertebrates have often focused on quantifying age-related changes in fecundity and mortality [3], but less often on physiological mechanisms that may contribute to such demographic ageing (e.g., [4,5,6]). One such candidate physiological mechanism is immune function, which plays a critical role in survival. Reduced immune function has been shown to negatively impact survival and reproduction [6,7,8]. The progressive deregulation of the immune system with age, termed immunosenescence, has been well studied in humans for both innate immunity (whose dysregulation with age can lead to chronic inflammation [9]), and acquired immunity, where the best studied changes are an increase in memory T cells and decrease in naïve T cells with advancing age (but here too, immunosenescence remains enigmatic [10]). However, age-specific changes in the immune system of long-lived, wild, non-mammalian populations are not well described in the literature, and studies focusing on reptile immunosenescence are even more rare (reviewed in [8]).
Comments
This article is published as Bronikowski, A.M., Hedrick, A.R., Kutz, G.A. et al. Sex-specific innate immunity and ageing in long-lived fresh water turtles (Kinosternon flavescens: Kinosternidae). Immun Ageing 20, 11 (2023). https://doi.org/10.1186/s12979-023-00335-x. Posted with permission.

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